Abstract
It is common practice to examine motor unit (MU) activity according to mean firing rate (MFR) and action potential amplitude (MUAPAMP) vs. recruitment threshold (RT) relationships during isometric trapezoidal contractions. However, it is unknown whether the rate of torque development during the linearly increasing torque phase affects the activity of MUs during such contractions. Sixteen healthy males and females performed two isometric trapezoidal muscle actions at 40% of maximum voluntary contraction (MVC), one at a rate of torque development of 5% MVC/s (SLOW40) and one at 20% MVC/s (FAST40) during the linearly increasing torque phase. Surface electromyography (EMG) was recorded from the vastus lateralis (VL) via a 5-pin surface array sensor and decomposed into action potential trains of individual MUs, yielding MFRs and MUAPAMP which were regressed against RT separately for each contraction. Surface EMG amplitude recorded from leg extensors and flexors was used to quantify muscle activation and coactivation. MFR vs. RT relationship slopes were more negative (P = 0.003) for the SLOW40 (− 0.491 ± 0.101 pps/%MVC) than FAST40 (− 0.322 ± 0.109 pps/%MVC) and the slopes of the MUAPAMP vs. RT relationships (P = 0.022, SLOW40 = 0.0057 ± 0.0021 mV/%MVC, FAST40 = 0.0041 ± 0.0023 mV/%MVC) and muscle activation of the extensors (P < 0.001, SLOW40 = 36.3 ± 7.82%, FAST40 = 34.0 ± 6.26%) were greater for SLOW40 than FAST40. MU firing rates were lower and action potential amplitudes were larger in relation to recruitment thresholds for a contraction performed at a slower rate compared to a faster rate of isometric torque development. Differences in MU activity can exist as a function of rate of torque development during commonly performed isometric trapezoidal contractions.
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References
Adam A, De Luca CJ (2005) Firing rates of motor units in human vastus lateralis muscle during fatiguing isometric contractions. J Appl Physiol 99:268–280. https://doi.org/10.1152/japplphysiol.01344.2004
Colquhoun RJ, Magrini MA, Haun CT et al (2018a) Muscle phenotype is related to motor unit behavior of the vastus lateralis during maximal isometric contractions. Physiol Rep 6:e13636. https://doi.org/10.14814/phy2.13636
Colquhoun RJ, Tomko PM, Magrini MA et al (2018b) The influence of input excitation on the inter- and intra-day reliability of the motor unit firing rate versus recruitment threshold relationship. J Neurophysiol 120:3131–3139
Contessa P, De Luca CJ, Kline JC (2016) The compensatory interaction between motor unit firing behavior and muscle force during fatigue. J Neurophysiol 116:1579–1585. https://doi.org/10.1152/jn.00347.2016
Contessa P, Letizi J, De Luca G, Kline JC (2018) Contribution from motor unit firing adaptations and muscle coactivation during fatigue. J Neurophysiol 119:2186–2193. https://doi.org/10.1152/jn.00766.2017
Conwit RA, Stashuk D, Tracy B et al (1999) The relationship of motor unit size, firing rate and force. Clin Neurophysiol 110:1270–1275. https://doi.org/10.1016/S1388-2457(99)00054-1
De Luca CJ, Contessa P (2012) Hierarchical control of motor units in voluntary contractions. J Neurophysiol 107:178–195. https://doi.org/10.1152/jn.00961.2010
De Luca CJ, Contessa P (2015) Biomechanical benefits of the onion-skin motor unit control scheme. J Biomech 48:195–203
De Luca CJ, Erim Z (1994) Common drive of motor units in regulation of muscle force. Trends Neurosci 17:299–305
De Luca CJ, Hostage EC (2010) Relationship between firing rate and recruitment threshold of motoneurons in voluntary isometric contractions. J Neurophysiol 104:1034–1046. https://doi.org/10.1152/jn.01018.2009
De Luca CJ, Kline JC (2012) Influence of proprioceptive feedback on the firing rate and recruitment of motoneurons. J Neural Eng 9:016007. https://doi.org/10.1088/1741-2560/9/1/016007
De Luca CJ, Foley PJ, Erim Z (1996) Motor unit control properties in constant-force isometric contractions. J Neurophysiol 76:1503–1516. https://doi.org/10.1152/jn.1996.76.3.1503
De Luca CJ, Adam A, Wotiz R et al (2006) Decomposition of surface EMG signals. J Neurophysiol 96:1646–1657. https://doi.org/10.1152/jn.00009.2006
Del Vecchio A, Negro F, Felici F, Farina D (2018) Distribution of muscle fibre conduction velocity for representative samples of motor units in the full recruitment range of the tibialis anterior muscle. Acta Physiol 222:e12930. https://doi.org/10.1111/apha.12930
Del Vecchio A, Casolo A, Negro F et al (2019) The increase in muscle force after 4 weeks of strength training is mediated by adaptations in motor unit recruitment and rate coding. J Physiol. https://doi.org/10.1113/jp277250
Desmedt JE, Godaux E (1977) Ballistic contractions in man: characteristic recruitment pattern of single motor units of the tibialis anterior muscle. J Physiol 264:673–693. https://doi.org/10.1113/jphysiol.1977.sp011689
Dorfman LJ, Howard JE, McGill KC (1990) Triphasic behavioral response of motor units to submaximal fatiguing exercise. Muscle Nerve 13:621–628. https://doi.org/10.1002/mus.880130711
Erim Z, Beg MF, Burke DT, de Luca CJ (1999) Effects of aging on motor-unit control properties. J Neurophysiol 82:2081–2091. https://doi.org/10.1152/jn.1999.82.5.2081
Farina D, Holobar A, Merletti R, Enoka RM (2010) Decoding the neural drive to muscles from the surface electromyogram. Clin Neurophysiol 121:1616–1623. https://doi.org/10.1016/j.clinph.2009.10.040
Goldberg LJ, Derfler B (1977) Relationship among recruitment order, spike amplitude, and twitch tension of single motor units in human masseter muscle. J Neurophysiol 40:879–890. https://doi.org/10.1152/jn.1977.40.4.879
Guo J-Y, Zheng Y-P, Xie H-B, Chen X (2010) Continuous monitoring of electromyography (EMG), mechanomyography (MMG), sonomyography (SMG) and torque output during ramp and step isometric contractions. Med Eng Phys 32:1032–1042. https://doi.org/10.1016/j.medengphy.2010.07.004
Hakansson CH (1956) Conduction velocity and amplitude of the action potential as related to circumference in the isolated fibre of frog muscle. Acta Physiol Scand 37:14–34. https://doi.org/10.1111/j.1748-1716.1956.tb01338.x
Henneman E (1957) Relation between size of neurons and their susceptibility to discharge. Science 126:1345–1347
Herda TJ, Siedlik JA, Trevino MA et al (2015) Motor unit control strategies of endurance- versus resistance-trained individuals. Muscle Nerve 52:832–843. https://doi.org/10.1002/mus.24597
Herda TJ, Trevino MA, Sterczala AJ et al (2019) Muscular strength and power are correlated with motor unit action potential amplitudes, but not myosin heavy chain isoforms in sedentary males and females. J Biomech 86:251–255. https://doi.org/10.1016/j.jbiomech.2019.01.050
Horita T, Ishiko T (1987) Relationships between muscle lactate accumulation and surface EMG activities during isokinetic contractions in man. Eur J Appl Physiol 56:18–23. https://doi.org/10.1007/BF00696370
Hu X, Rymer WZ, Suresh NL (2013a) Motor unit pool organization examined via spike-triggered averaging of the surface electromyogram. J Neurophysiol 110:1205–1220. https://doi.org/10.1152/jn.00301.2012
Hu X, Rymer WZ, Suresh NL (2013b) Assessment of validity of a high-yield surface electromyogram decomposition. J NeuroEng Rehabil 10:99. https://doi.org/10.1186/1743-0003-10-99
Hu X, Rymer WZ, Suresh NL (2013c) Reliability of spike triggered averaging of the surface electromyogram for motor unit action potential estimation. Muscle Nerve 48:557–570. https://doi.org/10.1002/mus.23819
Jubeau M, Gondin J, Martin A et al (2010) Differences in twitch potentiation between voluntary and stimulated quadriceps contractions of equal intensity. Scand J Med Sci Sports 20:e56–e62. https://doi.org/10.1111/j.1600-0838.2009.00897.x
Kennedy PM, Cresswell AG (2001) The effect of muscle length on motor-unit recruitment during isometric plantar flexion in humans. Exp Brain Res 137:58–64. https://doi.org/10.1007/s002210000623
Klein CS, Ivanova TD, Rice CL, Garland SJ (2001) Motor unit discharge rate following twitch potentiation in human triceps brachii muscle. Neurosci Lett 316:153–156. https://doi.org/10.1016/S0304-3940(01)02389-8
Kouzaki M, Shinohara M, Fukunaga T (2000) Decrease in maximal voluntary contraction by tonic vibration applied to a single synergist muscle in humans. J Appl Physiol 89:1420–1424. https://doi.org/10.1152/jappl.2000.89.4.1420
Maffiuletti NA, Aagaard P, Blazevich AJ et al (2016) Rate of force development: physiological and methodological considerations. Eur J Appl Physiol 116:1091–1116. https://doi.org/10.1007/s00421-016-3346-6
Martinez-Valdes E, Negro F, Falla D et al (2018) Surface electromyographic amplitude does not identify differences in neural drive to synergistic muscles. J Appl Physiol 124:1071–1079. https://doi.org/10.1152/japplphysiol.01115.2017
Masakado Y, Noda Y, Nagata M et al (1994) Macro-EMG and motor unit recruitment threshold: differences between the young and the aged. Neurosci Lett 179:1–4. https://doi.org/10.1016/0304-3940(94)90920-2
Masakado Y, Akaboshi K, Nagata M et al (1995) Motor unit firing behavior in slow and fast contractions of the first dorsal interosseous muscle of healthy men. Electroencephalogr Clin Neurophysiol 97:290–295
McManus L, Hu X, Rymer WZ et al (2016) Muscle fatigue increases beta-band coherence between the firing times of simultaneously active motor units in the first dorsal interosseous muscle. J Neurophysiol 115:2830–2839. https://doi.org/10.1152/jn.00097.2016
Miller JD, Herda TJ, Trevino MA et al (2017a) Age-related differences in twitch properties and muscle activation of the first dorsal interosseous. Clin Neurophysiol 128:925–934. https://doi.org/10.1016/j.clinph.2017.03.032
Miller JD, Herda TJ, Trevino MA et al (2017b) Time-related changes in firing rates are influenced by recruitment threshold and twitch force potentiation in the first dorsal interosseous: recruitment threshold, potentiation and motor unit firing rates. Exp Physiol 102:950–961. https://doi.org/10.1113/EP086262
Miller JD, Sterczala AJ, Trevino MA, Herda TJ (2018) Examination of muscle composition and motor unit behavior of the first dorsal interosseous of normal and overweight children. J Neurophysiol 119:1902–1911. https://doi.org/10.1152/jn.00675.2017
Miller JD, Sterczala AJ, Trevino MA et al (2019) Motor unit action potential amplitudes and firing rates during repetitive muscle actions of the first dorsal interosseous in children and adults. Eur J Appl Physiol. https://doi.org/10.1007/s00421-019-04090-0
Milner-Brown HS, Stein RB (1975) The relation between the surface electromyogram and muscular force. J Physiol 246:549–569. https://doi.org/10.1113/jphysiol.1975.sp010904
Nawab SH, Chang S-S, De Luca CJ (2010) High-yield decomposition of surface EMG signals. Clin Neurophysiol 121:1602–1615. https://doi.org/10.1016/j.clinph.2009.11.092
Peng Y-L, Tenan MS, Griffin L (2018) Hip position and sex differences in motor unit firing patterns of the vastus medialis and vastus medialis oblique in healthy individuals. J Appl Physiol 124:1438–1446. https://doi.org/10.1152/japplphysiol.00702.2017
Pope ZK, Hester GM, Benik FM, DeFreitas JM (2016) Action potential amplitude as a noninvasive indicator of motor unit-specific hypertrophy. J Neurophysiol 115:2608–2614. https://doi.org/10.1152/jn.00039.2016
Potvin JR, Fuglevand AJ (2017) A motor unit-based model of muscle fatigue. PLoS Comput Biol 13:e1005581. https://doi.org/10.1371/journal.pcbi.1005581
Rattey J, Martin PG, Kay D et al (2006) Contralateral muscle fatigue in human quadriceps muscle: evidence for a centrally mediated fatigue response and cross-over effect. Pflüg Arch Eur J Physiol 452:199–207. https://doi.org/10.1007/s00424-005-0027-4
Seki K, Miyazaki Y, Watanabe M et al (1991) Surface electromyogram spectral characterization and motor unit activity during voluntary ramp contraction in men. Eur J Appl Physiol 63:165–172. https://doi.org/10.1007/BF00233842
Sterczala AJ, Herda TJ, Miller JD et al (2018a) Age-related differences in the motor unit action potential size in relation to recruitment threshold. Clin Physiol Funct Imaging 38:610–616. https://doi.org/10.1111/cpf.12453
Sterczala AJ, Miller JD, Trevino MA et al (2018b) Differences in the motor unit firing rates and amplitudes in relation to recruitment thresholds during submaximal contractions of the first dorsal interosseous between chronically resistance-trained and physically active men. Appl Physiol Nutr Metab. https://doi.org/10.1139/apnm-2017-0646
Stock MS, Beck TW, Defreitas JM (2012) Effects of fatigue on motor unit firing rate versus recruitment threshold relationships. Muscle Nerve 45:100–109. https://doi.org/10.1002/mus.22266
Tenan MS, Peng Y-L, Hackney AC, Griffin LK (2013) Menstrual cycle mediates vastus medialis and vastus medialis oblique muscle activity. Med Sci Sports Exerc 45:2151–2157. https://doi.org/10.1249/MSS.0b013e318299a69d
Tomko PM, Colquhoun RJ, Magrini MA et al (2018) Global electromyographic signal characteristics depend on maximal isometric contraction method in the knee extensors. J Electromyogr Kinesiol 42:111–116
Tracy BL, Enoka RM (2002) Older adults are less steady during submaximal isometric contractions with the knee extensor muscles. J Appl Physiol 92:1004–1012. https://doi.org/10.1152/japplphysiol.00954.2001
Trevino MA, Herda TJ, Fry AC et al (2016) Influence of the contractile properties of muscle on motor unit firing rates during a moderate-intensity contraction in vivo. J Neurophysiol 116:552–562. https://doi.org/10.1152/jn.01021.2015
Trevino MA, Sterczala AJ, Miller JD et al (2018) Sex-related differences in muscle size explained by amplitudes of higher-threshold motor unit action potentials and muscle fibre typing. Acta Physiol. https://doi.org/10.1111/apha.13151
Vander Linden DW, Kukulka CG, Soderberg GL (1991) The effect of muscle length on motor unit discharge characteristics in human tibialis anterior muscle. Exp Brain Res 84:210–218. https://doi.org/10.1007/BF00231776
Vila-Chã C, Falla D, Farina D (2010) Motor unit behavior during submaximal contractions following six weeks of either endurance or strength training. J Appl Physiol 109:1455–1466. https://doi.org/10.1152/japplphysiol.01213.2009
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The authors would like to thank the undergraduate research assistants who aided in the collection and analysis of data. We would also like to thank the subjects for their selfless participation.
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JDM and TJH developed the research design. CJL, MDG, KLS, MEW collected and analyzed data. JDM analyzed data, performed statistical procedures, and prepared the figures and manuscript. TJH aided in manuscript preparation. All authors edited the manuscript and approved the final version.
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New and Noteworthy: It is common practice to characterize motor unit activity during submaximal isometric trapezoidal contractions, however, it is unknown whether the rate of torque development during such contractions influences motor unit activity. The current study revealed larger action potential amplitudes and decreased firing rates in relation to recruitment thresholds for contractions performed with a slower compared to a faster rate of torque development, suggesting motor unit activity is altered by rate of torque development.
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Miller, J.D., Lund, C.J., Gingrich, M.D. et al. The effect of rate of torque development on motor unit recruitment and firing rates during isometric voluntary trapezoidal contractions. Exp Brain Res 237, 2653–2664 (2019). https://doi.org/10.1007/s00221-019-05612-0
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DOI: https://doi.org/10.1007/s00221-019-05612-0